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Disturbed Ca2+ Homeostasis in Muscle-Wasting Disorders

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Muscle Atrophy

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1088))

Abstract

Ca2+ is essential for proper structure and function of skeletal muscle. It not only activates contraction and force development but also participates in multiple signaling pathways. Low levels of Ca2+ restrain muscle regeneration by limiting the fusion of satellite cells. Ironically, sustained elevations of Ca2+ also result in muscle degeneration as this ion promotes high rates of protein breakdown. Moreover, transforming growth factors (TGFs) which are well known for controlling muscle growth also regulate Ca2+ channels. Thus, therapies focused on changing levels of Ca2+ and TGFs are promising for treating muscle-wasting disorders. Three principal systems govern the homeostasis of Ca2+, namely, excitation-contraction (EC) coupling, excitation-coupled Ca2+ entry (ECCE), and store-operated Ca2+ entry (SOCE). Accordingly, alterations in these systems can lead to weakness and atrophy in many hereditary diseases, such as Brody disease, central core disease (CCD), tubular aggregate myopathy (TAM), myotonic dystrophy type 1 (MD1), oculopharyngeal muscular dystrophy (OPMD), and Duchenne muscular dystrophy (DMD). Here, the interrelationship between all these molecules and processes is reviewed.

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References

  1. Franzini-Armstrong C (2018) The relationship between form and function throughout the history of excitation-contraction coupling. J Gen Physiol 150:189–210

    Article  PubMed  PubMed Central  Google Scholar 

  2. Konig S, Béguet A, Bader CR, Bernheim L (2006) The calcineurin pathway links hyperpolarization (Kir2.1)-induced Ca2+ signals to human myoblast differentiation and fusion. Development 133:3107–3114

    Article  CAS  PubMed  Google Scholar 

  3. Sacchetto R, Bovo E, Salviati L, Damiani E, Margreth A (2007) Glycogen synthase binds to sarcoplasmic reticulum and is phosphorylated by CaMKII in fast-twitch skeletal muscle. Arch Biochem Biophys 459:115–121

    Article  CAS  PubMed  Google Scholar 

  4. Costelli P, Reffo P, Penna F, Autelli R, Bonelli G, Baccino FM (2005) Ca(2+)-dependent proteolysis in muscle wasting. Int J Biochem Cell Biol 37:2134–2146

    Article  CAS  PubMed  Google Scholar 

  5. Al-Shanti N, Stewart CE (2009) Ca2+/calmodulin-dependent transcriptional pathways: potential mediators of skeletal muscle growth and development. Biol Rev Camb Philos Soc 84:637–652

    Article  PubMed  Google Scholar 

  6. Armstrong CM, Bezanilla FM, Horowicz P (1972) Twitches in the presence of ethylene glycol bis( −aminoethyl ether)-N,N’-tetracetic acid. Biochim Biophys Acta 267:605–608

    Article  CAS  Google Scholar 

  7. Miledi R, Parker I, Schalow G (1977) Measurement of calcium transients in frog muscle by the use of arsenazo III. Proceedings of the Royal Society of London. Series B Biol Sci 198:201–210

    Article  CAS  Google Scholar 

  8. Caputo C, Bezanilla F, Horowicz P (1984) Depolarization-contraction coupling in short frog muscle fibers. A voltage clamp study. J Gen Physiol 84:133–154

    Article  CAS  PubMed  Google Scholar 

  9. Schneider MF, Chandler WK (1973) Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature 242:244–246

    Article  CAS  PubMed  Google Scholar 

  10. Rios E, Brum G (1987) Involvement of dihydropyridine receptors in excitation-contraction coupling in skeletal muscle. Nature 325:717–720

    Article  CAS  PubMed  Google Scholar 

  11. Tanabe T, Beam KG, Powell JA, Numa S (1988) Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature 336:134–139

    Article  CAS  PubMed  Google Scholar 

  12. Inui M, Saito A, Fleischer S (1987) Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem 262:1740–1747

    CAS  PubMed  Google Scholar 

  13. Takekura H, Nishi M, Noda T, Takeshima H, Franzini-Armstrong C (1995) Abnormal junctions between surface membrane and sarcoplasmic reticulum in skeletal muscle with a mutation targeted to the ryanodine receptor. Proc Natl Acad Sci U S A 92:3381–3385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Beam KG, Knudson CM, Powell JA (1986) A lethal mutation in mice eliminates the slow calcium current in skeletal muscle cells. Nature 320:168–170

    Article  CAS  PubMed  Google Scholar 

  15. Takeshima H, Iino M, Takekura H, Nishi M, Kuno J, Minowa O, Takano H, Noda T (1994) Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene. Nature 369:556–559

    Article  CAS  PubMed  Google Scholar 

  16. Buck ED, Nguyen HT, Pessah IN, Allen PD (1997) Dyspedic mouse skeletal muscle expresses major elements of the triadic junction but lacks detectable ryanodine receptor protein and function. J Biol Chem 272:7360–7367

    Article  CAS  PubMed  Google Scholar 

  17. Dirksen RT, Beam KG (1999) Role of calcium permeation in dihydropyridine receptor function. Insights into channel gating and excitation-contraction coupling. J Gen Physiol 114:393–403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cherednichenko G, Hurne AM, Fessenden JD, Lee EH, Allen PD, Beam KG, Pessah IN (2004) Conformational activation of Ca2+ entry by depolarization of skeletal myotubes. Proc Natl Acad Sci U S A 101:15793–15798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bannister RA, Beam KG (2013) Ca(V)1.1: the atypical prototypical voltage-gated Ca2+ channel. Biochim Biophys Acta 1828:1587–1597

    Article  CAS  PubMed  Google Scholar 

  20. Bannister RA, Pessah IN, Beam KG (2009) The skeletal L-type Ca(2+) current is a major contributor to excitation-coupled Ca(2+) entry. J Gen Physiol 133:79–91

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Dirksen RT (2009) Checking your SOCCs and feet: the molecular mechanisms of Ca2+ entry in skeletal muscle. J Physiol Lond 587:3139–3147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Robin G, Allard B (2015) Voltage-gated Ca(2+) influx through L-type channels contributes to sarcoplasmic reticulum Ca(2+) loading in skeletal muscle. J Physiol Lond 593:4781–4797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Dayal A, Schrötter K, Pan Y, Föhr K, Melzer W, Grabner M (2017) The Ca2+influx through the mammalian skeletal muscle dihydropyridine receptor is irrelevant for muscle performance. Nat Commun 8:475

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Stathopulos PB, Ikura M (2013) Structural aspects of calcium-release activated calcium channel function. Channels 7:344–353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lyfenko AD, Dirksen RT (2008) Differential dependence of store-operated and excitation-coupled Ca2+ entry in skeletal muscle on STIM1 and Orai1. J Physiol Lond 586:4815–4824

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Stathopulos PB, Li G-Y, Plevin MJ, Ames JB, Ikura M (2006) Stored Ca2+ depletion-induced oligomerization of stromal interaction molecule 1 (STIM1) via the EF-SAM region: an initiation mechanism for capacitive Ca2+ entry. J Biol Chem 281:35855–35862

    Article  CAS  PubMed  Google Scholar 

  27. Launikonis BS, Murphy RM, Edwards JN (2010) Toward the roles of store-operated Ca2+ entry in skeletal muscle. Pflugers Archiv 460:813–823

    Article  CAS  PubMed  Google Scholar 

  28. Kurebayashi N, Ogawa Y (2001) Depletion of Ca2+ in the sarcoplasmic reticulum stimulates Ca2+ entry into mouse skeletal muscle fibres. J Physiol Lond 533:185–199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sztretye M, Geyer N, Vincze J, Al-Gaadi D, Oláh T, Szentesi P, Kis G, Antal M, Balatoni I, Csernoch L, Dienes B (2017) SOCE is important for maintaining sarcoplasmic calcium content and release in skeletal muscle fibers. Biophys J 113:2496–2507

    Article  CAS  PubMed  Google Scholar 

  30. Amthor H, Macharia R, Navarrete R, Schuelke M, Brown SC, Otto A, Voit T, Muntoni F, Vrbóva G, Partridge T, Zammit P, Bunger L, Patel K (2007) Lack of myostatin results in excessive muscle growth but impaired force generation. Proc Natl Acad Sci U S A 104:1835–1840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Brack AS, Rando TA (2012) Tissue-specific stem cells: lessons from the skeletal muscle satellite cell. Cell Stem Cell 10:504–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Randolph ME, Pavlath GK (2015) A muscle stem cell for every muscle: variability of satellite cell biology among different muscle groups. Front Aging Neurosci 7:190

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Crist C (2017) Emerging new tools to study and treat muscle pathologies: genetics and molecular mechanisms underlying skeletal muscle development, regeneration, and disease. J Pathol 241:264–272

    Article  PubMed  Google Scholar 

  34. Mitchell PO, Pavlath GK (2001) A muscle precursor cell-dependent pathway contributes to muscle growth after atrophy. Am J Physiol Cell Physiol 281:C1706–C1715

    Article  CAS  PubMed  Google Scholar 

  35. Liu W, Wei-LaPierre L, Klose A, Dirksen RT, Chakkalakal JV (2015) Inducible depletion of adult skeletal muscle stem cells impairs the regeneration of neuromuscular junctions. elife 4. https://doi.org/10.7554/eLife.09221

  36. Liu W, Klose A, Forman S, Paris ND, Wei-LaPierre L, Cortés-Lopéz M, Tan A, Flaherty M, Miura P, Dirksen RT, Chakkalakal JV (2017) Loss of adult skeletal muscle stem cells drives age-related neuromuscular junction degeneration. elife 6. https://doi.org/10.7554/eLife.26464

  37. Chen JCJ, Goldhamer DJ (2003) Skeletal muscle stem cells. Reprod Biol Endocrinol 1:101

    Article  PubMed  PubMed Central  Google Scholar 

  38. Parker MH, Seale P, Rudnicki MA (2003) Looking back to the embryo: defining transcriptional networks in adult myogenesis. Nat Rev Genet 4:497–507

    Article  CAS  PubMed  Google Scholar 

  39. Horsley V, Pavlath GK (2004) Forming a multinucleated cell: molecules that regulate myoblast fusion. Cells Tissues Organs 176:67–78

    Article  PubMed  Google Scholar 

  40. Benavides Damm T, Egli M (2014) Calcium’s role in mechanotransduction during muscle development. Cell Physiol Biochem 33:249–272

    Article  CAS  PubMed  Google Scholar 

  41. Phuong TTT, Yun Y-H, Kim SJ, Kang TM (2013) Positive feedback control between STIM1 and NFATc3 is required for C2C12 myoblast differentiation. Biochem Biophys Res Commun 430:722–728

    Article  CAS  PubMed  Google Scholar 

  42. Warnes DM, Tomas FM, Ballard FJ (1981) Increased rates of myofibrillar protein breakdown in muscle-wasting diseases. Muscle Nerve 4:62–66

    Article  CAS  PubMed  Google Scholar 

  43. Tong J, McCarthy TV, MacLennan DH (1999) Measurement of resting cytosolic Ca2+ concentrations and Ca2+ store size in HEK-293 cells transfected with malignant hyperthermia or central core disease mutant Ca2+ release channels. J Biol Chem 274:693–702

    Article  CAS  PubMed  Google Scholar 

  44. Avila G, O’Connell KM, Groom LA, Dirksen RT (2001) Ca2+ release through ryanodine receptors regulates skeletal muscle L-type Ca2+ channel expression. J Biol Chem 276:17732–17738

    Article  CAS  PubMed  Google Scholar 

  45. Vega AV, Ramos-Mondragón R, Calderón-Rivera A, Zarain-Herzberg A, Avila G (2011) Calcitonin gene-related peptide restores disrupted excitation-contraction coupling in myotubes expressing central core disease mutations in RyR1. J Physiol Lond 589:4649–4669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Filipova D, Henry M, Rotshteyn T, Brunn A, Carstov M, Deckert M, Hescheler J, Sachinidis A, Pfitzer G, Papadopoulos S (2018) Distinct transcriptomic changes in E14.5 mouse skeletal muscle lacking RYR1 or Cav1.1 converge at E18.5. PLoS One 13:e0194428

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Beam KG, Knudson CM (1988) Effect of postnatal development on calcium currents and slow charge movement in mammalian skeletal muscle. J Gen Physiol 91:799–815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Berthier C, Monteil A, Lory P, Strube C (2002) Alpha(1H) mRNA in single skeletal muscle fibres accounts for T-type calcium current transient expression during fetal development in mice. J Physiol Lond 539:681–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bijlenga P, Liu JH, Espinos E, Haenggeli CA, Fischer-Lougheed J, Bader CR, Bernheim L (2000) T-type alpha 1H Ca2+ channels are involved in Ca2+ signaling during terminal differentiation (fusion) of human myoblasts. Proc Natl Acad Sci U S A 97:7627–7632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Bidaud I, Monteil A, Nargeot J, Lory P (2006) Properties and role of voltage-dependent calcium channels during mouse skeletal muscle differentiation. J Muscle Res Cell Motil 27:75–81

    Article  CAS  PubMed  Google Scholar 

  51. Louis M, Zanou N, Van Schoor M, Gailly P (2008) TRPC1 regulates skeletal myoblast migration and differentiation. J Cell Sci 121:3951–3959

    Article  CAS  PubMed  Google Scholar 

  52. Darbellay B, Arnaudeau S, König S, Jousset H, Bader C, Demaurex N, Bernheim L (2009) STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. J Biol Chem 284:5370–5380

    Article  CAS  PubMed  Google Scholar 

  53. Shefer G, Yablonka-Reuveni Z, Schiaffino S, Partridge T (2008) The ins and outs of satellite cell Myogenesis: the role of the ruling growth factors. In: Skeletal muscle repair and regeneration. Springer, Dordrecht, pp 107–144

    Chapter  Google Scholar 

  54. McPherron AC, Lawler AM, Lee SJ (1997) Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387:83–90

    Article  CAS  PubMed  Google Scholar 

  55. Tsuchida K (2008) Targeting myostatin for therapies against muscle-wasting disorders. Curr Opin Drug Discov Devel 11:487–494

    CAS  PubMed  Google Scholar 

  56. Mejia-Luna L, Avila G (2004) Ca2+ channel regulation by transforming growth factor-beta 1 and bone morphogenetic protein-2 in developing mice myotubes. J Physiol Lond 559:41–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Katagiri T, Yamaguchi A, Komaki M, Abe E, Takahashi N, Ikeda T, Rosen V, Wozney JM, Fujisawa-Sehara A, Suda T (1994) Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J Cell Biol 127:1755–1766

    Article  CAS  PubMed  Google Scholar 

  58. Rossi AE, Dirksen RT (2006) Sarcoplasmic reticulum: the dynamic calcium governor of muscle. Muscle Nerve 33:715–731

    Article  CAS  PubMed  Google Scholar 

  59. Dowling JJ, Lawlor MW, Dirksen RT (2014) Triadopathies: an emerging class of skeletal muscle diseases. Neurotherapeutics 11:773–785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Voermans NC, Laan AE, Oosterhof A, van Kuppevelt TH, Drost G, Lammens M, Kamsteeg EJ, Scotton C, Gualandi F, Guglielmi V, van den Heuvel L, Vattemi G, van Engelen BG (2012) Brody syndrome: a clinically heterogeneous entity distinct from Brody disease: a review of literature and a cross-sectional clinical study in 17 patients. Neuromuscul Disord 22:944–954

    Article  CAS  PubMed  Google Scholar 

  61. Odermatt A, Taschner PE, Khanna VK, Busch HF, Karpati G, Jablecki CK, Breuning MH, MacLennan DH (1996) Mutations in the gene-encoding SERCA1, the fast-twitch skeletal muscle sarcoplasmic reticulum Ca2+ ATPase, are associated with Brody disease. Nat Genet 14:191–194

    Article  CAS  PubMed  Google Scholar 

  62. MacLennan DH, Loke JC (2002) Brody disease associated with defects in a calcium pump. In: Karpati G (ed) Structural and molecular basis of skeletal muscle disease. ISN Neuropath, Basel, pp 103–105

    Google Scholar 

  63. Guglielmi V, Vattemi G, Gualandi F, Voermans NC, Marini M, Scotton C, Pegoraro E, Oosterhof A, Kósa M, Zádor E, Valente EM, De Grandis D, Neri M, Codemo V, Novelli A, van Kuppevelt TH, Dallapiccola B, van Engelen BG, Ferlini A, Tomelleri G (2013) SERCA1 protein expression in muscle of patients with Brody disease and Brody syndrome and in cultured human muscle fibers. Mol Genet Metab 110:162–169

    Article  CAS  PubMed  Google Scholar 

  64. Karpati G, Charuk J, Carpenter S, Jablecki C, Holland P (1986) Myopathy caused by a deficiency of Ca2+−adenosine triphosphatase in sarcoplasmic reticulum (Brody’s disease). Ann Neurol 20:38–49

    Article  CAS  PubMed  Google Scholar 

  65. Benders AA, Veerkamp JH, Oosterhof A, Jongen PJ, Bindels RJ, Smit LM, Busch HF, Wevers RA (1994) Ca2+ homeostasis in Brody’s disease. A study in skeletal muscle and cultured muscle cells and the effects of dantrolene an verapamil. J Clin Investig 94:741–748

    Article  CAS  PubMed  Google Scholar 

  66. Fauré J, Lunardi J, Monnier N, Marty I (2014) Ryanodine receptor 1 and associated pathologies. In: Pathologies of calcium channels. Springer, Berlin/Heidelberg, pp 167–187

    Chapter  Google Scholar 

  67. Marty I, Fauré J (2016) Excitation-contraction coupling alterations in myopathies. J Neuromuscul Dis 3:443–453

    Article  PubMed  PubMed Central  Google Scholar 

  68. Jungbluth H (2007) Central core disease. Orphanet J Rare Dis 2:25

    Article  PubMed  PubMed Central  Google Scholar 

  69. Guerrero-Hernández A, Avila G, Rueda A (2014) Ryanodine receptors as leak channels. Eur J Pharmacol 739C:26–38

    Article  CAS  Google Scholar 

  70. Avila G, Dirksen RT (2001) Functional effects of central core disease mutations in the cytoplasmic region of the skeletal muscle ryanodine receptor. J Gen Physiol 118:277–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Avila G, O’Brien JJ, Dirksen RT (2001) Excitation--contraction uncoupling by a human central core disease mutation in the ryanodine receptor. Proc Natl Acad Sci U S A 98:4215–4220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Zvaritch E, Depreux F, Kraeva N, Loy RE, Goonasekera SA, Boncompagni S, Kraev A, Gramolini AO, Dirksen RT, Franzini-Armstrong C, Seidman CE, Seidman JG, Maclennan DH (2007) An Ryr1I4895T mutation abolishes Ca2+ release channel function and delays development in homozygous offspring of a mutant mouse line. Proc Natl Acad Sci U S A 104:18537–18542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Loy RE, Orynbayev M, Xu L, Andronache Z, Apostol S, Zvaritch E, MacLennan DH, Meissner G, Melzer W, Dirksen RT (2011) Muscle weakness in Ryr1I4895T/WT knock-in mice as a result of reduced ryanodine receptor Ca2+ ion permeation and release from the sarcoplasmic reticulum. J Gen Physiol 137:43–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Monnier N, Ferreiro A, Marty I, Labarre-Vila A, Mezin P, Lunardi J (2003) A homozygous splicing mutation causing a depletion of skeletal muscle RYR1 is associated with multi-minicore disease congenital myopathy with ophthalmoplegia. Hum Mol Genet 12:1171–1178

    Article  CAS  PubMed  Google Scholar 

  75. Zhou H, Brockington M, Jungbluth H, Monk D, Stanier P, Sewry CA, Moore GE, Muntoni F (2006) Epigenetic allele silencing unveils recessive RYR1 mutations in core myopathies. Am J Hum Genet 79:859–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Zhou H, Lillis S, Loy RE, Ghassemi F, Rose MR, Norwood F, Mills K, Al-Sarraj S, Lane RJ, Feng L, Matthews E, Sewry CA, Abbs S, Buk S, Hanna M, Treves S, Dirksen RT, Meissner G, Muntoni F, Jungbluth H (2010) Multi-minicore disease and atypical periodic paralysis associated with novel mutations in the skeletal muscle ryanodine receptor (RYR1) gene. Neuromuscul Disord 20:166–173

    Article  PubMed  PubMed Central  Google Scholar 

  77. Cacheux M, Blum A, Sébastien M, Wozny AS, Brocard J, Mamchaoui K, Mouly V, Roux-Buisson N, Rendu J, Monnier N, Krivosic R, Allen P, Lacour A, Lunardi J, Fauré J, Marty I (2015) Functional characterization of a central Core disease RyR1 mutation (p.Y4864H) associated with quantitative defect in RyR1 protein. J Neuromuscul Dis 2:421–432

    Article  PubMed  PubMed Central  Google Scholar 

  78. Chen W, Koop A, Liu Y, Guo W, Wei J, Wang R, MacLennan DH, Dirksen RT, Chen SRW (2017) Reduced threshold for store overload-induced Ca2+release is a common defect of RyR1 mutations associated with malignant hyperthermia and central core disease. Biochem J 474:2749–2761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Lee CS, Hanna AD, Wang H, Dagnino-Acosta A, Joshi AD, Knoblauch M, Xia Y, Georgiou DK, Xu J, Long C, Amano H, Reynolds C, Dong K, Martin JC, Lagor WR, Rodney GG, Sahin E, Sewry C, Hamilton SL (2017) A chemical chaperone improves muscle function in mice with a RyR1 mutation. Nat Commun 8:14659

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Messina S, Hartley L, Main M, Kinali M, Jungbluth H, Muntoni F, Mercuri E (2004) Pilot trial of salbutamol in central core and multi-minicore diseases. Neuropediatrics 35:262–266

    Article  CAS  PubMed  Google Scholar 

  81. Böhm J, Chevessier F, Maues De Paula A, Koch C, Attarian S, Feger C, Hantaï D, Laforêt P, Ghorab K, Vallat JM, Fardeau M, Figarella-Branger D, Pouget J, Romero NB, Koch M, Ebel C, Levy N, Krahn M, Eymard B, Bartoli M, Laporte J (2013) Constitutive activation of the calcium sensor STIM1 causes tubular-aggregate myopathy. Am J Hum Genet 92:271–278

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Böhm J, Chevessier F, Koch C, Peche GA, Mora M, Morandi L, Pasanisi B, Moroni I, Tasca G, Fattori F, Ricci E, Pénisson-Besnier I, Nadaj-Pakleza A, Fardeau M, Joshi PR, Deschauer M, Romero NB, Eymard B, Laporte J (2014) Clinical, histological and genetic characterisation of patients with tubular aggregate myopathy caused by mutations in STIM1. J Med Genet 51:824–833

    Article  PubMed  CAS  Google Scholar 

  83. Hedberg C, Niceta M, Fattori F, Lindvall B, Ciolfi A, D’Amico A, Tasca G, Petrini S, Tulinius M, Tartaglia M, Oldfors A, Bertini E (2014) Childhood onset tubular aggregate myopathy associated with de novo STIM1 mutations. J Neurol 261:870–876

    Article  PubMed  Google Scholar 

  84. Okuma H, Saito F, Mitsui J, Hara Y, Hatanaka Y, Ikeda M, Shimizu T, Matsumura K, Shimizu J, Tsuji S, Sonoo M (2016) Tubular aggregate myopathy caused by a novel mutation in the cytoplasmic domain of STIM1. Neurol Genet 2:e50

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  85. Walter MC, Rossius M, Zitzelsberger M, Vorgerd M, Müller-Felber W, Ertl-Wagner B, Zhang Y, Brinkmeier H, Senderek J, Schoser B (2015) 50 years to diagnosis: autosomal dominant tubular aggregate myopathy caused by a novel STIM1 mutation. Neuromuscul Disord 25:577–584

    Article  PubMed  Google Scholar 

  86. Nesin V, Wiley G, Kousi M, Ong EC, Lehmann T, Nicholl DJ, Suri M, Shahrizaila N, Katsanis N, Gaffney PM, Wierenga KJ, Tsiokas L (2014) Activating mutations in STIM1 and ORAI1 cause overlapping syndromes of tubular myopathy and congenital miosis. Proc Natl Acad Sci U S A 111:4197–4202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Endo Y, Noguchi S, Hara Y, Hayashi YK, Motomura K, Miyatake S, Murakami N, Tanaka S, Yamashita S, Kizu R, Bamba M, Goto Y, Matsumoto N, Nonaka I, Nishino I (2015) Dominant mutations in ORAI1 cause tubular aggregate myopathy with hypocalcemia via constitutive activation of store-operated Ca2+ channels. Hum Mol Genet 24:637–648

    Article  CAS  PubMed  Google Scholar 

  88. Garibaldi M, Fattori F, Riva B, Labasse C, Brochier G, Ottaviani P, Sacconi S, Vizzaccaro E, Laschena F, Romero NB, Genazzani A, Bertini E, Antonini G (2017) A novel gain-of-function mutation in ORAI1 causes late-onset tubular aggregate myopathy and congenital miosis. Clin Genet 91:780–786

    Article  CAS  PubMed  Google Scholar 

  89. Barone V, Del Re V, Gamberucci A, Polverino V, Galli L, Rossi D, Costanzi E, Toniolo L, Berti G, Malandrini A, Ricci G, Siciliano G, Vattemi G, Tomelleri G, Pierantozzi E, Spinozzi S, Volpi N, Fulceri R, Battistutta R, Reggiani C, Sorrentino V (2017) Identification and characterization of three novel mutations in the CASQ1 gene in four patients with tubular aggregate myopathy. Hum Mutat 38:1761–1773

    Article  CAS  PubMed  Google Scholar 

  90. Jacobs AE, Benders AA, Oosterhof A, Veerkamp JH, van Mier P, Wevers RA, Joosten EM (1990) The calcium homeostasis and the membrane potential of cultured muscle cells from patients with myotonic dystrophy. Biochim Biophys Acta 1096:14–19

    Article  CAS  PubMed  Google Scholar 

  91. Benders AA, Groenen PJ, Oerlemans FT, Veerkamp JH, Wieringa B (1997) Myotonic dystrophy protein kinase is involved in the modulation of the Ca2+ homeostasis in skeletal muscle cells. J Clin Investig 100:1440–1447

    Article  CAS  PubMed  Google Scholar 

  92. Santoro M, Piacentini R, Masciullo M, Bianchi MLE, Modoni A, Podda MV, Ricci E, Silvestri G, Grassi C (2014) Alternative splicing alterations of Ca2+ handling genes are associated with Ca2+ signal dysregulation in myotonic dystrophy type 1 (DM1) and type 2 (DM2) myotubes. Neuropathol Appl Neurobiol 40:464–476

    Article  CAS  PubMed  Google Scholar 

  93. Carrell ST, Carrell EM, Auerbach D, Pandey SK, Bennett CF, Dirksen RT, Thornton CA (2016) Dmpk gene deletion or antisense knockdown does not compromise cardiac or skeletal muscle function in mice. Hum Mol Genet 25:4328–4338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Rodríguez R, Hernández-Hernández O, Magaña JJ, González-Ramírez R, García-López ES, Cisneros B (2015) Altered nuclear structure in myotonic dystrophy type 1-derived fibroblasts. Mol Biol Rep 42:479–488

    Article  PubMed  CAS  Google Scholar 

  95. Tang ZZ, Yarotskyy V, Wei L, Sobczak K, Nakamori M, Eichinger K, Moxley RT, Dirksen RT, Thornton CA (2012) Muscle weakness in myotonic dystrophy associated with misregulated splicing and altered gating of ca(V)1.1 calcium channel. Hum Mol Genet 21:1312–1324

    Article  CAS  PubMed  Google Scholar 

  96. Kimura T, Nakamori M, Lueck JD, Pouliquin P, Aoike F, Fujimura H, Dirksen RT, Takahashi MP, Dulhunty AF, Sakoda S (2005) Altered mRNA splicing of the skeletal muscle ryanodine receptor and sarcoplasmic/endoplasmic reticulum Ca2+-ATPase in myotonic dystrophy type 1. Hum Mol Genet 14:2189–2200

    Article  CAS  PubMed  Google Scholar 

  97. Calado A, Tomé FM, Brais B, Rouleau GA, Kühn U, Wahle E, Carmo-Fonseca M (2000) Nuclear inclusions in oculopharyngeal muscular dystrophy consist of poly(A) binding protein 2 aggregates which sequester poly(A) RNA. Hum Mol Genet 9:2321–2328

    Article  CAS  PubMed  Google Scholar 

  98. Abu-Baker A, Rouleau GA (2007) Oculopharyngeal muscular dystrophy: recent advances in the understanding of the molecular pathogenic mechanisms and treatment strategies. Biochim Biophys Acta 1772:173–185

    Article  CAS  PubMed  Google Scholar 

  99. Trollet C, Gidaro T, Klein P, Périé S, Butler-Browne G, Lacau St Guily J (1993) Oculopharyngeal muscular dystrophy. In: Adam MP, Ardinger HH, Pagon RA, Wallace SE, LJH B, Stephens K, Amemiya A (eds) GeneReviews® [internet]. University of Washington, Seattle

    Google Scholar 

  100. Corbeil-Girard L-P, Klein AF, Sasseville AM-J, Lavoie H, Dicaire MJ, Saint-Denis A, Pagé M, Duranceau A, Codère F, Bouchard JP, Karpati G, Rouleau GA, Massie B, Langelier Y, Brais B (2005) PABPN1 overexpression leads to upregulation of genes encoding nuclear proteins that are sequestered in oculopharyngeal muscular dystrophy nuclear inclusions. Neurobiol Dis 18:551–567

    Article  CAS  PubMed  Google Scholar 

  101. García-Castañeda M, Vega AV, Rodríguez R, Montiel-Jaen MG, Cisneros B, Zarain-Herzberg A, Avila G (2017) Functional impact of an oculopharyngeal muscular dystrophy mutation in PABPN1. J Physiol Lond 595:4167–4187

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  102. Périé S, Mamchaoui K, Mouly V, Blot S, Bouazza B, Thornell L-E, St Guily JL, Butler-Browne G (2006) Premature proliferative arrest of cricopharyngeal myoblasts in oculo-pharyngeal muscular dystrophy: therapeutic perspectives of autologous myoblast transplantation. Neuromuscul Disord 16:770–781

    Article  PubMed  Google Scholar 

  103. Wang Q, Bag J (2006) Ectopic expression of a polyalanine expansion mutant of poly(A)-binding protein N1 in muscle cells in culture inhibits myogenesis. Biochem Biophys Res Commun 340:815–822

    Article  CAS  PubMed  Google Scholar 

  104. Apponi LH, Corbett AH, Pavlath GK (2013) Control of mRNA stability contributes to low levels of nuclear poly(A) binding protein 1 (PABPN1) in skeletal muscle. Skelet Muscle 3:23

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  105. Turner PR, Westwood T, Regen CM, Steinhardt RA (1988) Increased protein degradation results from elevated free calcium levels found in muscle from mdx mice. Nature 335:735–738

    Article  CAS  PubMed  Google Scholar 

  106. Franco A, Lansman JB (1990) Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature 344:670–673

    Article  CAS  PubMed  Google Scholar 

  107. Franco-Obregón A, Lansman JB (1994) Mechanosensitive ion channels in skeletal muscle from normal and dystrophic mice. J Physiol Lond 481(Pt 2):299–309

    Article  PubMed  PubMed Central  Google Scholar 

  108. Saüc S, Frieden M (2017) Neurological and motor disorders: TRPC in the skeletal muscle. Adv Exp Med Biol 993:557–575

    Article  PubMed  Google Scholar 

  109. Edwards JN, Friedrich O, Cully TR, von Wegner F, Murphy RM, Launikonis BS (2010) Upregulation of store-operated Ca2+ entry in dystrophic mdx mouse muscle. Am J Phys Cell Phys 299:C42–C50

    Article  CAS  Google Scholar 

  110. Zhao X, Moloughney JG, Zhang S, Komazaki S, Weisleder N (2012) Orai1 mediates exacerbated ca(2+) entry in dystrophic skeletal muscle. PLoS One 7:e49862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Goonasekera SA, Davis J, Kwong JQ, Accornero F, Wei-LaPierre L, Sargent MA, Dirksen RT, Molkentin JD (2014) Enhanced Ca2+ influx from STIM1-Orai1 induces muscle pathology in mouse models of muscular dystrophy. Hum Mol Genet 23:3706–3715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Burr AR, Molkentin JD (2015) Genetic evidence in the mouse solidifies the calcium hypothesis of myofiber death in muscular dystrophy. Cell Death Differ 22:1402–1412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Spinazzola JM, Kunkel LM (2016) Pharmacological therapeutics targeting the secondary defects and downstream pathology of Duchenne muscular dystrophy. Expert Opin Orphan Drugs 4:1179–1194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Malerba A, Kang JK, McClorey G, Saleh AF, Popplewell L, Gait MJ, Wood MJ, Dickson G (2012) Dual Myostatin and dystrophin exon skipping by Morpholino nucleic acid oligomers conjugated to a cell-penetrating peptide is a promising therapeutic strategy for the treatment of Duchenne muscular dystrophy. Mol Ther-Nucleic Acids 1:e62

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. St Andre M, Johnson M, Bansal PN, Wellen J, Robertson A, Opsahl A, Burch PM, Bialek P, Morris C, Owens J (2017) A mouse anti-myostatin antibody increases muscle mass and improves muscle strength and contractility in the mdx mouse model of Duchenne muscular dystrophy and its humanized equivalent, domagrozumab (PF-06252616), increases muscle volume in cynomolgus monkeys. Skelet Muscle 7:25

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  116. Smith RC, Lin BK (2013) Myostatin inhibitors as therapies for muscle wasting associated with cancer and other disorders. Curr Opin Support Palliat Care 7:352–360

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

The lab has been supported by CONACyT. I thank Lizbeth Mejía-Luna for help in preparing Fig. 14.2.

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The author declares no competing financial interests.

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  1. Department of Biochemistry, Cinvestav, México City, Mexico

    Guillermo Avila

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Correspondence to Guillermo Avila .

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  1. Cardiac Regeneration and Ageing Lab, Institute of Cardiovascular Sciences, School of Life Science, Shanghai University, Shanghai, China

    Junjie Xiao

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Avila, G. (2018). Disturbed Ca2+ Homeostasis in Muscle-Wasting Disorders. In: Xiao, J. (eds) Muscle Atrophy. Advances in Experimental Medicine and Biology, vol 1088. Springer, Singapore. https://doi.org/10.1007/978-981-13-1435-3_14

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